How Not to Be Turned into a Zombie

Abstract

The emerald jewel wasp (Ampulex compressa) is renowned for its ability to zombify the American cockroach (Periplaneta americana) with a sting to the brain. When the venom takes effect, the cockroach becomes passive and can be led by its antenna into a hole, where the wasp deposits an egg and then seals the exit with debris. The cockroach has the ability to walk, run, or fly if properly stimulated, but it does not try to escape as it is slowly eaten alive by the developing wasp larva. Although the composition and effects of the wasp's venom have been investigated, no studies have detailed how cockroaches might prevent this grim fate. Here it is shown that many cockroaches deter wasps with a vigorous defense. Successful cockroaches elevated their bodies, bringing their neck out of reach, and kicked at the wasp with their spiny hind legs, often striking the wasp's head multiple times. Failing this, the elevated, "on-guard" position allowed cockroaches to detect and evade the wasp's lunging attack. If grasped, the cockroaches parried the stinger with their legs, used a "stiff-arm" defense to hold back the stinger, and could stab at, and dislodge, the wasp with tibial spines. Lastly, cockroaches bit at the abdomen of wasps delivering the brain sting. An aggressive defense from the outset was most successful. Thus, for a cockroach not to become a zombie, the best strategy is: be vigilant, protect your throat, and strike repeatedly at the head of the attacker.

Keywords: Cockroach; Defense; Escape response; Evolution; Insects; Mechanosensation; Parasitoid; Wasps.

Fig. 1

A jewel wasp (Ampulex compressa) attacking an American cockroach (Periplaneta Americana). a Jewel wasps begin their attack by firmly grasping the plate-like pronotum of the cockroach with their mandibles. b After having paralyzed the front legs with a first sting into the first thoracic ganglion (not shown), the second sting is made into the head and brain of the cockroach.

Fig. 2

The stilt-standing defensive posture of the cockroach. a Schematized dorsal view of a typical cockroach posture, with the wasp's target (the pronotum) indicated with a red arrow. b Schematized stilt-standing posture with the legs and one antenna oriented toward the approaching wasp. c The cockroaches commonly turned away from the wasp, allowing for a kicking defense with the powerful hind legs. d Side view of a cockroach in a typical posture. e Side view of stilt-standing in response to a wasp, illustrating the elevation of the cockroach's body. f Stilt-standing while orienting the legs and one antenna toward the cockroach. g Stilt-standing after turning to position the wasp behind, illustrating the cockroach's body angled away from the wasp. In this stance, the pronotum is distant and raised away from the wasp.

Fig. 3

Kicking defense by the cockroach. a Schematized sequence of movements (red arrows) during the kick. The hind leg is raised and extended rostrally, and then swept back through the target, often projecting the wasp many centimeters away. b Frames captured from a video showing a defensive kick by a cockroach that impacts the wasp on the head and propels it away (top view). c Frames captured from a video showing a kick with a similar result (side view). Note the dorsal extension of the leg during the windup phase. d Ventral view of a defensive kick, with the cockroach holding on to the top of the chamber.

Fig. 4

Timing and elicitation of a kick. a Schematic illustration of the hind leg's position every millisecond for the swing phase of a kick. The positions were taken from the trial shown in clip 4 of online supplementary Movie S1. Note that the movement of the cockroach's body is not illustrated; rather, the leg's positions are relative to the initial body position. b Close view of a kick as filmed with a camera attached to a microscope. Just prior to the kick, the wasp's antenna deflects a single tibial spine (insets; red arrows). See clip 5 of online supplementary Movie S1 for the full trial.

Fig. 5

Escape responses elicited by a wasp's lunge. a–c Schematic illustration of a cockroach's escape, starting from a stilt-standing position (movements shown with red arrows). As the wasp lunges for the pronotum, contact is often made with one of the cockroach's legs or antennae, followed by a short-latency turn by the cockroach. d Frames captured from a video showing a wasp's lunge for the pronotum of a stilt-standing cockroach, and simultaneously deflecting a tibial spine of one of the cockroach's legs (insets; red arrows). The subsequent escape response moves the pronotum with only milliseconds to spare. See online supplementary Movie S2, clip 1. e A wasp lunges for the pronotum of a stilt-standing cockroach but hits the antenna with its mandibles (red arrow). Note that the roach and the wasp are holding on to the upper surface of the chamber. See online supplementary Movie S2, clip 2. f A wasp lunges for the pronotum of a stilt-standing cockroach but hits the antenna with its antenna (red arrow), followed by a short-latency turn by the cockroach.

Fig. 6

Escape responses elicited by a wasp's grasp to the pronotum. a Schematic illustration of successful escape after a pronotum grasp. If not already elicited, an escape response at this point was always triggered. The rapid turn sometimes dislodged the wasp (red arrows) but more often failed. b Frames captured from a video showing a wasp's dislodgment by a sudden turn. See online supplementary Movie S2, clip 10. c Frames captured from a video showing a wasp's dislodgment from turning. See online supplementary Movie S2, clip 11.

Fig. 7

Use of tibial spines to dislodge a wasp. a Schematic illustration of a cockroach using the tibial spines on the midleg to dislodge a grasping wasp. The leg is drawn forward, pressed against the wasp, and then drawn backwards, while the body is simultaneously rotated away (red arrows). b Frames captured from a video showing the use of tibial spines (red arrows) to dislodge a wasp. See online supplementary Movie S3, clip 1. c Frames captured from a video showing the use of tibial spines to dislodge a wasp. See online supplementary Movie S3, clip 5.

Fig. 8

Stiff-arm defense and biting. a Schematic illustration. The cockroaches often brought one or more legs up against the wasp and lodged the spines against the abdominal joint or along the abdomen, making it difficult for the wasp to sting. b Frame captured from a video showing the position of the midleg (red arrow) holding back the wasp's abdomen. See online supplementary Movie S4 for this and additional examples. c The cockroaches often raked the tibial spines repeatedly against the wasp during the struggle (red arrow), and occasionally lodged the spines in between the abdominal segments. This provided purchase for pushing the abdomen and stinger away from the thorax. See online supplementary Movie S5 for this and additional examples. d Frame captured from a video showing a cockroach attempting to bite the wasp's abdomen during the sting. In this case, the cockroach had lodged its spines between the abdominal segments and thus used its foreleg to bring the abdomen briefly between its mandibles; however, it was apparently unable to damage the smooth, hard cuticle. See online supplementary Movie S5 for this and other examples.

Fig. 9

Characteristic wasp posture during stinging. When delivering a sting, the wasps usually held their limbs up and away from the cockroach, in a pose reminiscent of a fencer. Presumably the similarity is in both form and function, as the wasp's delicate legs might otherwise be damaged by the cockroach's powerful jaws.